Interactions between age, stress and insulin on cognition: Implications for alzheimer's disease

Neuropsychopharmacology

Volumn 35, Issue 8, 2010, Pages 1664-1673

  Solas, Maite ^a   Aisa, Bárbara ^a   Mugueta, María C ^b   Del Río, Joaquín ^a   Tordera, Rosa M ^a   Ramírez, María J ^a  

^a UNIVERSITY OF NAVARRA   (Spain)

^b UNIVERSITY CLINIC OF NAVARRA   (Spain)

Author keywords

Amyloidogenic route; ARC; ERK2; Glucocorticoids; Hippocampus; Maternal separation

Indexed keywords

AMYLOID PRECURSOR PROTEIN; BETA SECRETASE 1; GLYCOGEN SYNTHASE KINASE 3BETA; INSULIN; INSULIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE B; TAU PROTEIN;

AGING; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DEPRESSION; EARLY LIFE STRESS; FORCED SWIMMING TEST; HIPPOCAMPUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LOCOMOTION; MALE; MATERNAL DEPRIVATION; MAZE TEST; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; RECOGNITION; STRESS; WEIGHT GAIN;

AGING; AMYLOID BETA-PROTEIN; ANIMALS; ANIMALS, NEWBORN; BRAIN-DERIVED NEUROTROPHIC FACTOR; COGNITION DISORDERS; CORTICOSTERONE; CYTOSKELETAL PROTEINS; DEPRESSION; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION REGULATION; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INSULIN; INSULIN-LIKE GROWTH FACTOR I; MALE; MATERNAL DEPRIVATION; MAZE LEARNING; MOTOR ACTIVITY; NERVE TISSUE PROTEINS; NEUROPSYCHOLOGICAL TESTS; PEPTIDE FRAGMENTS; PITUITARY-ADRENAL SYSTEM; PREGNANCY; RATS; RATS, WISTAR; RECEPTOR, INSULIN; RECOGNITION (PSYCHOLOGY); RNA, MESSENGER; SIGNAL TRANSDUCTION; STATISTICS, NONPARAMETRIC; STRESS, PSYCHOLOGICAL; SWIMMING;

EID: 77953614413     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/npp.2010.13     Document Type: Article

References (66)

1. Aisa B, Tordera R, Lasheras B, Del Ŕio J, Raḿirez MJ (2007). Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology 32: 256-266.
2. Amatruda JM, Livingston JN, Lockwood DH (1985). Cellular mechanisms in selected states of insulin resistance: human obesity, glucocorticoid excess, and chronic renal failure. Diabetes Metab Rev 1: 293-317.
3. Berger-Sweeney J, McPhie DL, Arters JA, Greenan J, Oster-Granite ML, Neve RL (1999). Impairments in learning and memory accompanied by neurodegeneration in mice transgenic for the carboxyl-terminus of the amyloid precursor protein. Mol Brain Res 66: 150-162.
4. Berton O, Nestler EJ (2006). New approaches to antidepressant drug discovery: beyond monoamines. Nat Rev Neurosci 7: 137-151.
5. Born J, Ditschuneit I, Schreiber M, Dodt C, Fehm HL (1995). Effects of age and gender on pituitary-adrenocortical responsiveness in humans. Eur J Endocrinol 132: 705-711.
6. Brown MW, Aggleton JP (2001). Recognition memory: what are the roles of the perirhinal cortex and hippocampus? Nat Rev Neurosci 2: 51-61.
7. Catania C, Sotiropoulos I, Silva R, Onofri C, Breen KC, Sousa N et al (2009). The amyloidogenic potential and behavioral correlates of stress. Mol Psychiatry 14: 95-105.
8. Christensen R, Marcussen AB, Wörtwein G, Knudsen GM, Aznar S (2008). Abeta(1-42) injection causes memory impairment, lowered cortical and serum BDNF levels, and decreased hippocampal 5-HT(2A) levels. Exp Neurol 210: 164-171.
9. Csernansky JG, Dong H, Fagan AM, Wang L, Xiong C, Holtzman DM et al (2006). Plasma cortisol and progression of dementia in subjects with Alzheimer-type dementia. Am J Psychiatry 163: 2164-2169.
10. Davis S, Laroche S (2006). Mitogen-activated protein kinase/extracellular regulated kinase signaling and memory stabilization: a review. Genes Brain Behav 5: 61-72.
11. De Felice FG, Vieira MN, Bomfim TR, Decker H, Velasco PT, Lambert MP et al (2009). Protection of synapses against Alzheimer's-linked toxins: insulin signaling prevents the pathogenic binding of Abeta oligomers. Proc Natl Acad Sci USA 106: 1971-1976.
12. Delaunay F, Khan A, Cintra A, Davani B, Ling ZC, Andersson A et al (1997). Pancreatic beta cells are important targets for the diabetogenic effects of glucocorticoids. J Clin Invest 100: 2094-2098.
13. Dhikav V, Anand KS (2007). Glucocorticoids may initiate Alzheimer's disease: a potential therapeutic role for mifepristone (RU-486). Med Hypotheses 68: 1088-1092.
14. Diez-Ariza M, Redondo C, Garcia-Alloza M, Lasheras B, Del Rio J, Ramirez MJ (2003). Flumazenil and tacrine increase the effectiveness of ondansetron on scopolamine-induced impairment of spatial learning in rats. Psychopharmacology 169: 35-41.
15. Duman RS, Monteggia LM (2006). A neurotrophic model for stress-related mood disorders. Biol Psychiatry 59: 1116-1127.
16. Dupont J, LeRoith D (2001). Insulin and insulin-like growth factor I receptors: similarities and differences in signal transduction. Horm Res 55: 22-26.
17. Eckel-Mahan KL, Phan T, Han S, Wang H, Chan GC, Scheiner ZS et al. (2008). Circadian oscillation of hippocampal MAPK activity and cAMP: implications for memory persistence. Nat Neurosci 11: 1074-1082.
18. Elgh E, Lindqvist Astot A, Fagerlund M, Eriksson S, Olsson T, Näsman B (2006). Cognitive dysfunction, hippocampal atrophy and glucocorticoid feedback in Alzheimer's disease. Biol Psychiatry 59: 155-161.
19. English JD, Sweatt JD (1996). Activation of p42 mitogen-activated protein kinase in hippocampal long term potentiation. J Biol Chem 271: 24329-24332.
20. Green KN, Billings LM, Roozendaal B, McGaugh JL, LaFerla FM (2006). Glucocorticoids increase amyloid-beta and tau pathology in a mouse model of Alzheimer's disease. J Neurosci 26: 9047-9056.
21. Guzowski JF, Lyford GL, Stevenson GD, Houston FP, McGaugh JL, Worley PF et al (2000). Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J Neurosci 20: 3993-4001.
22. Hartmann A, Veldhuis JD, Deuschle M, Standhardt H, Heuser I (1997). Twenty-four hour cortisol release profiles in patients with Alzheimer's and Parkinson's disease compared to normal controls: ultradian secretory pulsatility and diurnal variation. Neurobiol Aging 18: 285-289.
23. Hauger RL, Thrivikraman KV, Plotsky PM (1994). Age-related alterations of hypothalamic-pituitary-adrenal axis function in male Fischer 344 rats. Endocrinology 134: 1528-1536.
24. Heim C, Nemeroff CB (1999). The impact of early adverse experiences on brain systems involved in the pathophysiology of anxiety and affective disorders. Biol Psychiatry 46: 1509-1522.
25. Heim C, Nemeroff CB (2001). The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatry 49: 1023-1039.
26. Huot RL, Plotsky PM, Lenox RH, McNamara RK (2002). Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats. Brain Res 950: 52-63.
27. Jeong YH, Park CH, Yoo J, Shin KY, Ahn SM, Kim HS et al (2006). Chronic stress accelerates learning and memory impairments and increases amyloid deposition in APPV717I-CT100 trans-genic mice, an Alzheimer's disease model. FASEB J 20: 729-731.
28. Kendler KS, Karkowski LM, Prescott CA (1999). Causal relationship between stressful life events and the onset of major depression. Am J Psychiatry 156: 837-841.
29. Kulstad JJ, McMillan PJ, Leverenz JB, Cook DG, Green PS, Peskind ER et al (2005). Effects of chronic glucocorticoid administration on insulin-degrading enzyme and amyloid-beta peptide in the aged macaque. J Neuropathol Exp Neurol 64: 139-146.
30. Kurochkin IV, Goto S (1994). Alzheimer's b-amyloid peptide specifically interacts with and is degraded by insulin degrading enzyme. FEBS Lett 345: 33-37.
31. Ladd CO, Huot RL, Thrivikraman KV, Nemeroff CB, Meaney MJ, Plotsky PM (2000). Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog Brain Res 122: 81-103.
32. Ladd CO, Huot RL, Thrivikraman KV, Nemeroff CB, Plotsky PM (2004). Long-term adaptations in glucocorticoid receptor and mineralocorticoid receptor mRNA and negative feedback on the hypothalamo-pituitary-adrenal axis following neonatal maternal separation. Biol Psychiatry 55: 367-375.
33. Lambillotte C, Gilon P, Henquin JC (1997). Direct glucocorticoid inhibition of insulin secretion: an in vitro study of dexametha-sone effects in mouse islets. J Clin Invest 99: 414-423.
34. Lehmann J, Feldon J (2000). Long-term biobehavioral effects of maternal separation in the rat: consistent or confusing? Rev Neurosci 11: 383-408.
35. Lupien SJ, de Leon M, de Santi S, Convit A, Tarshish C, Nair NP et al (1998). Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nat Neurosci 1: 69-73.
36. Magariños AM, McEwen BS (2000). Experimental diabetes in rats causes hippocampal dendritic and synaptic reorganization and increased glucocorticoid reactivity to stress. Proc Natl Acad Sci USA 97: 11056-11061.
37. McEwen BS (2002). Sex, stress and the hippocampus: allostasis, allostatic load and the aging process. Neurobiol Aging 23: 921-939.
38. Miller DB, O'Callaghan JP (2005). Aging, stress and the hippocampus. Ageing Res Rev 4: 123-140.
39. Montaron MF, Drapeau E, Dupret D, Kitchener P, Aurousseau C, Le Moal M et al (2006). Lifelong corticosterone level determines age-related decline in neurogenesis and memory. Neurobiol Aging 27: 645-654.
40. Nalbantoglu J, Tirado-Santiago G, Lahsaini A, Poirier J, Goncalves O, Verge G et al (1997). Impaired learning and LTP in mice expressing the carboxy terminus of the Alzheimer amyloid precursor protein. Nature 387: 500-505.
41. Oitzl MS, Workel JO, Fluttert M, Frösch F, De Kloet ER (2000). Maternal deprivation affects behaviour from youth to senescence: amplification of individual differences in spatial learning and memory in senescent Brown Norway rats. Eur J Neurosci 12: 3771-3780.
42. Oster-Granite ML, McPhie DL, Greenan J, Neve RL (1996). Age-dependent neuronal and synaptic degeneration in mice trans-genic for the C terminus of the amyloid precursor protein. J Neurosci 16: 6732-6741.
43. Ownby RL, Crocco E, Acevedo A, John V, Loewenstein D (2006). Depression and risk for Alzheimer disease: systematic review, meta-analysis, and metaregression analysis. Arch Gen Psychiatry 63: 530-538.
44. Paxinos G, Watson C (1982). The Rat Brain in Stereotaxic Coordinates. Academic Press: San Diego.
45. Porsolt RD, Le Pichon M, Jalfre M (1977). Depression: a new animal model sensitive to antidepressant treatments. Nature 266: 730-732.
46. Qiu WQ, Walsh DM, Ye Z, Vekrellis K, Zhang J, Podlisny MB et al (1998). Insulin-degrading enzyme regulates extracellular levels of amyloid b-protein by degradation. J Biol Chem 273: 32730-32738.
47. Roceri M, Hendriks W, Racagni G, Ellenbroek BA, Riva A (2002). Early maternal deprivation reduces the expression of BDNF and NMDA receptor subunits in rat hippocampus. Mol Psychiatry 7: 609-616.
48. Sambamurti K, Kinsey R, Maloney B, Ge YW, Lahiri DK (2004). Gene structure and organization of the human beta-secretase (BACE) promoter. FASEB J 18: 1034-1036.
49. Sapolsky RM, Krey LC, McEwen BS (1983). The adrenocortical stress-response in the aged male rat: impairment of recovery from stress. Exp Gerontol 18: 55-64.
50. Sapolsky RM (1985). Glucocorticoid toxicity in the hippocampus: temporal aspects of neuronal vulnerability. Brain Res 359: 300-305.
51. Sapolsky RM, Pulsinelli WA (1985). Glucocorticoids potentiate ischemic injury to neurons: therapeutic implications. Science 229: 1397-1400.
52. Sapolsky RM, Krey LC, McEwen BS (1986). The neuroendocrinol-ogy of stress and aging: the glucocorticoid cascade hypothesis. Endocr Rev 7: 284-301.
53. Sapolsky RM, Meaney MJ (1986). Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Res 396: 64-76.
54. Schubert M, Gautam D, Surjo D, Ueki K, Baudler S, Schubert D et al (2004). Role for neuronal insulin resistance in neurode-generative diseases. Proc Natl Acad Sci USA 101: 3100-3105.
55. Shaikh TH, O'Connor RJ, Pierpont ME, McGrath J, Hacker AM, Nimmakayalu M et al (2007). Low copy repeats mediate distal chromosome 22q11.2 deletions: sequence analysis predicts breakpoint mechanisms. Genome Res 17: 482-491.
56. Steen E, Terry BM, Rivera EJ, Cannon JL, Neely TR, Tavares R et al (2005). Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer's diseaseFis this type 3 diabetes? J Alzheimers Dis 7: 63-80.
57. Stranahan AM, Arumugam TV, Cutler RG, Lee K, Egan JM, Mattson MP (2008). Diabetes impairs hippocampal function through glucocorticoid-mediated effects on new and mature neurons. Nat Neurosci 11: 309-317.
58. Townsend M, Mehta T, Selkoe DJ (2007). Soluble Abeta inhibits specific signal transduction cascades common to the insulin receptor pathway. J Biol Chem 282: 33305-33312.
59. Van der Heide LP, Ramakers GM, Smidt MP (2006). Insulin signaling in the central nervous system: learning to survive. Prog Neurobiol 79: 205-221.
60. Warner-Schmidt JL, Duman RS (2006). Hippocampal neuro-genesis: opposing effects of stress and antidepressant treatment. Hippocampus 16: 239-249.
61. Wigger A, Neumann ID (1999). Periodic maternal deprivation induces gender-dependent alterations in behavioral and neuro-endocrine responses to emotional stress in adult rats. Physiol Behav 66: 293-302.
62. Wilson RS, Barnes LL, Bennett DA, Li Y, Bienias JL, Mendes de Leon CF et al (2005). Proneness to psychological distress and risk of Alzheimer disease in a biracial community. Neurology 64: 380-382.
63. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME (1995). Opposing effects of ERK and JNK-p38 MAP kinases on apop-tosis. Science 270: 1326-1331.
64. Yankner BA, Dawes LR, Fisher S, Villa-Komaroff L, Oster-Granite ML et al (1989). Neurotoxicity of a fragment of the amyloid precursor associated with Alzheimer's disease. Science 245: 417-420.
65. Zhao WQ, De Felice FG, Fernandez S, Chen H, Lambert MP, Quon MJ et al (2008). Amyloid beta oligomers induce impairment of neuronal insulin receptors. FASEB J 22: 246-260.
66. Zheng F, Luo Y, Wang H (2009). Regulation of brain-derived neurotrophic factor-mediated transcription of the immediate early gene Arc by intracellular calcium and calmodulin. J Neurosci Res 87: 380-392.